Original Article
Rocky Mountain Spotted Fever from an Unexpected Tick Vector in Arizona
N Engl J Med 2005; 353:587-594August 11, 2005
- Abstract
Background
Rocky Mountain spotted fever is a life-threatening, tick-borne disease caused by Rickettsia rickettsii. This disease is rarely reported in Arizona, and the principal vectors, Dermacentor species ticks, are uncommon in the state. From 2002 through 2004, a focus of Rocky Mountain spotted fever was investigated in rural eastern Arizona.
Methods
We obtained blood and tissue specimens from patients with suspected Rocky Mountain spotted fever and ticks from patients' homesites. Serologic, molecular, immunohistochemical, and culture assays were performed to identify the causative agent. On the basis of specific laboratory criteria, patients were classified as having confirmed or probable Rocky Mountain spotted fever infection.
Results
A total of 16 patients with Rocky Mountain spotted fever infection (11 with confirmed and 5 with probable infection) were identified. Of these patients, 13 (81 percent) were children 12 years of age or younger, 15 (94 percent) were hospitalized, and 2 (12 percent) died. Dense populations of Rhipicephalus sanguineus ticks were found on dogs and in the yards of patients' homesites. All patients with confirmed Rocky Mountain spotted fever had contact with tick-infested dogs, and four had a reported history of tick bite preceding the illness. R. rickettsii DNA was detected in nonengorged R. sanguineus ticks collected at one home, and R. rickettsii isolates were cultured from these ticks.
Conclusions
This investigation documents the presence of Rocky Mountain spotted fever in eastern Arizona, with common brown dog ticks (R. sanguineus) implicated as a vector of R. rickettsii. The broad distribution of this common tick raises concern about its potential to transmit R. rickettsii in other settings.
Media in This Article
Figure 1
The Principal Recognized Tick Vectors of Rickettsia rickettsii.Figure 2
Immunohistochemical Staining of Skin-Biopsy and Autopsy Specimens from Patients with Rocky Mountain Spotted Fever.Article Activity
- Article
Rocky mountain spotted fever, which is caused by Rickettsia rickettsii, is a life-threatening, tick-borne disease that occurs throughout much of the United States. Case fatality rates can be as high as 20 percent in untreated patients.1,2 The principal recognized vectors of R. rickettsii are Dermacentor variabilis (the American dog tick) (Figure 1AFigure 1
The Principal Recognized Tick Vectors of Rickettsia rickettsii.) in the eastern and central United States and D. andersoni (the Rocky Mountain wood tick) (Figure 1B) in the western United States. Both types of tick feed on small mammals, which may harbor R. rickettsii. D. variabilis, the most common tick associated with Rocky Mountain spotted fever, also commonly feeds on dogs.3 Another common tick throughout the world that feeds on dogs, Rhipicephalus sanguineus (the brown dog tick) (Figure 1C), has not previously been reported to be a natural vector for Rocky Mountain spotted fever in the United States.Rocky Mountain spotted fever is rarely reported in Arizona, and the expected Dermacentor species vectors are not commonly found in the state.4 From 1981 through 2001, only three cases of Rocky Mountain spotted fever were reported for the entire state.1,2 However, from 2002 through 2004, Rocky Mountain spotted fever was identified in 16 patients from rural eastern Arizona. In this report, we describe that outbreak and summarize the clinical, epidemiologic, and ecologic findings that implicate R. sanguineus as a newly recognized vector for R. rickettsii in the region.
Methods
Laboratory Testing
Serum, whole-blood, or tissue specimens for diagnostic testing were obtained from patients in whom Rocky Mountain spotted fever was suspected because they had a fever of 38°C (100.5°F) or higher, a maculopapular rash, or both. Serum samples were tested with the use of indirect immunofluorescence assays for IgG and IgM antibodies reactive with R. rickettsii; the assays were performed at commercial laboratories and at the Centers for Disease Control and Prevention (CDC) in Atlanta.5 Tissue specimens were evaluated at the CDC with the use of an immunohistochemical stain to detect the spotted-fever–group rickettsiae.6 DNA was extracted from whole blood, serum sediment, or tissue with the use of a commercial kit (QIAamp DNA Mini Kit, Qiagen) and assayed in a nested polymerase-chain-reaction (PCR) assay at the CDC to amplify a fragment of the 17-kD antigen gene (htrA) of the spotted-fever–group rickettsiae.7 Samples that were positive on this assay were further tested with the use of a PCR assay targeting a portion of the rOmpA gene, and species identification of R. rickettsii was confirmed through direct DNA sequencing or restriction-fragment–length polymorphism analysis of the amplified products.8,9 A confirmed case of Rocky Mountain spotted fever was defined as one in which there was at least one of the following findings: a change by a factor of four or more in the antibody titer between paired serum specimens; a skin-biopsy or autopsy-tissue specimen that was positive on immunohistochemical staining for spotted-fever–group rickettsiae; R. rickettsii DNA-positive serum, whole blood, or tissue; and isolation in culture on Vero E6 cells of R. rickettsii from patient samples.10,11 A probable case of Rocky Mountain spotted fever was defined as one in which there was a reciprocal IgM or IgG antibody titer of 64 or more in a single serum sample or in paired samples that did not show a change by a factor of four or more in antibody titer.
Case Investigations
From 2003 through 2004, patients with Rocky Mountain spotted fever were identified through active surveillance at the regional hospital serving the affected communities. Reviews of medical charts provided information about these patients. Interviews with patients and family members assessed possible tick exposures, descriptions of the home environment, and contact with dogs. Patients in whom the onset of illness occurred before 2003 were identified through anecdotal reports and their cases documented through the retrospective review of medical charts.
Investigation of Dogs and Ticks from Patients' Homesites
Serum samples were obtained from dogs owned by patients and tested with the use of an immunofluorescence assay for IgG antibodies reactive to R. rickettsii. Ticks were collected from patient homesites with the use of dry ice as an attractant, hand picking from various substrates, and flannel flags dragged over vegetation and bare ground during September 2003, June 2004, and September 2004. All ticks were identified with the use of standard taxonomic keys. Quantitative PCR12 and DNA sequencing were used to detect R. rickettsii DNA in ticks, as described above. A subgroup of ticks were homogenized and inoculated onto Vero E6 cells.10,11 R. rickettsii–positive cultures were confirmed with the use of PCR and DNA sequencing.
Results
Epidemiologic and Clinical Case Findings
During the period from June 2002 through October 2004, 11 confirmed and 5 probable Rocky Mountain spotted fever infections were identified in a 6700-km2 (2600 square-mile) region of rural eastern Arizona. Ten patients (62 percent) were male, and 13 (81 percent) were 12 years of age or younger (median age, 7.5 years; range, 9 months to 68 years) (Table 1Table 1
Characteristics of Patients with Confirmed or Probable Rocky Mountain Spotted Fever Infections in Arizona, 2002 through 2004.). Seven patients resided in a single small community (population, approximately 2148) in this circumscribed region. Nine additional patients resided in a second community (population, approximately 10,000) located about 50 miles away. None of the patients or their families reported having traveled outside the region in the two weeks before the onset of illness. The average annual incidence (from 2002 through 2004) of Rocky Mountain spotted fever among children and adolescents 19 years of age or younger in the region was 1800 cases per million persons.Laboratory, epidemiologic, and clinical features of the 16 patients with confirmed or probable Rocky Mountain spotted fever are presented in Table 1. Cases were confirmed through one or more of the following methods: the detection of spotted-fever–group rickettsiae in skin-biopsy or tissue specimens on immunohistochemical staining (five patients) (Figure 2Figure 2
Immunohistochemical Staining of Skin-Biopsy and Autopsy Specimens from Patients with Rocky Mountain Spotted Fever.), seroconversion (eight patients), or PCR amplification of R. rickettsii DNA in serum, blood, skin, or lung tissue (four patients). R. rickettsii isolates were cultured from tissue specimens from two patients.All patients had contact with tick-infested dogs. Four patients (25 percent) had a known history of tick bite, and a R. sanguineus nymph was found attached to Patient 3. Fifteen patients (94 percent) had fever of 38°C (100.5°F) or higher, and 15 (94 percent) had maculopapular rashes, of which 13 involved the palms or soles during the course of illness. Other reported signs and symptoms included cough or sore throat (five patients), nausea or vomiting (five), myalgia (four), diarrhea (three), abdominal pain (two), and headache (two). Common laboratory findings included elevated hepatic aminotransferase levels (aspartate aminotransferase, >36 U per liter; alanine aminotransferase, >52 U per liter; nine patients), hyponatremia (serum sodium, <130 mmol per liter; eight patients), and thrombocytopenia (platelet count, <130,000 per cubic millimeter; four patients). Fifteen patients (94 percent) required hospitalization, and six (38 percent) required treatment in an intensive care unit. Patients 2 and 7, in whom Rocky Mountain spotted fever was not initially suspected and in whom treatment with doxycycline was not started or was initiated late in the clinical course of illness, died from the infection. The overall case fatality rate, calculated over three years, was 12 percent.
In addition to the 16 cases presented here, we retrospectively identified 3 additional patients from the same communities in whom illness began during 2001 and whom we suspected had Rocky Mountain spotted fever. All three patients had an illness clinically compatible with a diagnosis of Rocky Mountain spotted fever, and two reported a tick bite before the onset of illness. Disseminated intravascular coagulopathy developed in a two-year-old patient, who died, but serum and tissue specimens were not available for testing. A serum specimen obtained in 2003 from a 3-year-old patient showed titers of IgG antibody to R. rickettsii of 2048, and a specimen obtained in 2004 from a 23-year-old patient showed reciprocal titers of IgG and IgM to R. rickettsii of 32 and 1024, respectively, suggesting that the prior illnesses in these patients were probably Rocky Mountain spotted fever.
Investigation of Dogs and Ticks from Patients' Homesites
The communities had large populations of dogs, many of which roamed freely among homesites. Serum specimens obtained from four dogs owned by Patients 3, 4, and 6 showed high titers of IgG antibodies reactive with R. rickettsii (≥16,384), indicating previous exposure to spotted-fever–group rickettsiae. Sixty-five partially or fully engorged R. sanguineus ticks were collected from dogs owned by some patients. R. rickettsii DNA was detected in one engorged adult R. sanguineus tick collected from a dog owned by Patient 3, and an isolate of R. rickettsii was cultured from this tick.
During the environmental assessment, nonengorged R. sanguineus ticks — 24 larvae, 753 nymphs, and 269 adults — were collected from the domestic environment of patients with confirmed Rocky Mountain spotted fever and from some neighboring community homesites. No Dermacentor species or ticks of other genera were found. Ticks were found in the immediate domestic environment, including in cracks in the stucco walls of homesites (Figure 3AFigure 3
The Domestic Environment of Patients' Homesites with Abundant Rhipicephalus sanguineus Populations. and Figure 3B), in the crawl spaces under houses (Figure 3C), and in discarded upholstered furniture that was placed outdoors and on which children and dogs were observed to rest. R. rickettsii DNA was detected with the use of PCR in 2 of 70 nonengorged adult R. sanguineus ticks (3 percent) collected from the domestic environment of Patient 7 and corroborated by culture isolation of R. rickettsii from these same ticks.Discussion
Our investigation of a focus of Rocky Mountain spotted fever in Arizona provides evidence that the common brown dog tick, R. sanguineus, may be a vector for Rocky Mountain spotted fever in some areas of the United States. Several lines of evidence strongly implicate R. sanguineus as the tick vector responsible for this hyperendemic focus of Rocky Mountain spotted fever. Ticks in all life stages were distributed abundantly in the environments in and around many of the patients' homes, and R. rickettsii was detected on PCR and cultured from engorged and nonengorged R. sanguineus adult ticks collected from patients' homesites. Neither D. variabilis nor D. andersoni ticks, the primary vectors for Rocky Mountain spotted fever in the United States, were found despite repeated entomologic evaluations at several times during the year. The hot, dry environmental conditions found in eastern Arizona (Figure 3D) are not likely to support tick species other than R. sanguineus. The precise factors responsible for the magnitude of this outbreak remain to be determined, but they are probably related to locally high densities of R. sanguineus ticks and their close association with dogs and their proximity to humans in this area.
R. sanguineus is found worldwide and is widely distributed across North America, feeding primarily on dogs during each of its life stages.13 R. sanguineus ticks bite humans infrequently, but immature R. sanguineus ticks are more likely than adults to feed on humans and have been shown to bite humans when their numbers are abundant.14-17 Indeed, an R. sanguineus nymph was removed from a patient during this investigation, demonstrating that there is parasitism of humans by this tick species in this setting. Investigators in the 1930s determined in the laboratory that R. sanguineus was a vector of R. rickettsii and capable of efficient transstadial transmission (between developmental stages) and transovarial transmission of this agent.18 Studies in Mexico during the 1940s identified R. sanguineus as a vector for pathogenic spotted-fever–group rickettsiae proven to be antigenically identical to R. rickettsii.19,20 In addition, R. sanguineus is the principal vector of R. conorii, a pathogenic spotted-fever–group rickettsia species that causes disease in Europe, Africa, and Asia.21 In these areas, a high prevalence of infestation by R. sanguineus ticks and close proximity of dogs and humans are risk factors for rickettsial infection.21-25 Although previously suggested,26,27 a role for this tick in the natural dynamics of transmission of R. rickettsii in the United States has not been demonstrated before this outbreak.
In this investigation, all patients reported contact with tick-infested dogs. Dogs serve as important transport hosts by carrying infected ticks close to their owners, as illustrated by numerous published reports of concurrent cases of Rocky Mountain spotted fever in dogs and their owners.28-31 A possible role for dogs as natural reservoirs of R. rickettsii has not been thoroughly studied. Rickettsemia has been shown to be maintained in dogs for 6 to 10 days after experimental infection with R. rickettsii,32-34 which could serve as a source of infection for feeding ticks. The factors contributing to the establishment of R. rickettsii in this new setting in Arizona may include dogs' functioning as reservoirs for the transmission of R. rickettsii among R. sanguineus ticks, the persistence of R. rickettsii within the tick population, or both. These possibilities should be explored more fully.
The incidence of Rocky Mountain spotted fever among children in this region (1800 cases per million persons 19 years of age or younger) is extremely high as compared with the average national annual incidence of only 5.6 cases per million persons for the same age group (National Electronic Telecommunication System for Surveillance, CDC, 1997–2002, unpublished data). There may be specific risk factors associated with the transmission of Rocky Mountain spotted fever that are unique to this age group; children were reported to associate closely with tick-infested dogs and to play frequently on discarded furniture that was found to harbor ticks. Young children may also have difficulty recognizing or reporting tick bites, which can result in prolonged attachment of the ticks and, possibly, increased rates of transmission of R. rickettsii.
It may not be possible to generalize the ecologic circumstances responsible for the infestation of R. sanguineus ticks in the Arizona communities to other regions of the United States where Rocky Mountain spotted fever is endemic; however, our investigation demonstrates that R. sanguineus can play a more important part in the natural history of R. rickettsii and the epidemiology of Rocky Mountain spotted fever than has been previously appreciated. The domestic habitat and broad distribution of R. sanguineus in the Western Hemisphere are a cause for concern about human exposure to this vector and the introduction of Rocky Mountain spotted fever into areas where it has not previously been recognized. Our findings suggest that other outbreaks and hyperendemic foci of Rocky Mountain spotted fever should be more closely investigated to determine whether R. sanguineus has a role in the transmission of the disease.
We are indebted to Brian Johnson, Jeff Dickson, Rudy Ethelbah, David Yost, Alma Chavez, Cheryl Mason, Mary Foote, Laura Banks, Donald Reece, Elizabeth Melius, John Peabody, Steve Piontkowski, Karen Heath, Kelly Robinson, and Kathy Chamberlin for assistance with the outbreak investigations and environmental assessments; to Jeannette Guarner and Wun-Ju Shieh of the National Center for Infectious Diseases (NCID), Centers for Disease Control and Prevention (CDC), for immunohistochemical diagnostics; to Elizabeth Bosserman, Maria Zambrano, Christina Sandema, Danielle Ross, and John Moriarity of the NCID for laboratory processing of ticks; to Elisabeth Lawaczeck and Craig Levy of the Arizona Department of Health Services and Staci Murphy, John Krebs, J. Erin Staples, Herbert Thompson, and James LeDuc of the NCID for assistance with and helpful insights during the investigation; and to Gary Hettrick, Rocky Mountain Laboratories, and James Gathany, CDC, for the use of their photographs.
Source Information
From the National Center for Infectious Diseases, Division of Viral and Rickettsial Diseases (L.J.D., W.L.N., C.D.P., D.M.B., M.E.E., G.A.D., M.L.L., J.S., S.R.Z., D.L.S., J.H.M.) and the Epidemic Intelligence Service, Office of Workforce and Career Development (L.J.D.), the Centers for Disease Control and Prevention, Atlanta; the Indian Health Service, Whiteriver Service Unit, Whiteriver, Ariz. (M.S.T.); and the Indian Health Service, National Epidemiology Program, Albuquerque, N.M. (J.E.C.).
Address reprint requests to Dr. Demma at the Centers for Disease Control and Prevention, 1600 Clifton Rd., MS D63, Atlanta, GA 30333, or at ldemma@cdc.gov.
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